Connective auxin transport contributes to strigolactone-mediated shoot branching control independent of the transcription factor BRC1

Abstract

The shoot systems of plants are built by the action of the primary shoot apical meristem, established during embryogenesis. In the axil of each leaf produced by the primary meristem, secondary axillary shoot apical meristems are established. The dynamic regulation of the activity of these axillary meristems gives shoot systems their extraordinary plasticity of form. The ability of plants to activate or repress these axillary meristems appropriately requires communication between meristems that is environmentally sensitive. The transport network of the plant hormone auxin has long been implicated as a central player in this tuneable communication system, with other systemically mobile hormones, such as strigolactone and cytokinin, acting in part by modulating auxin transport. Until recently, the polar auxin transport stream, which provides a high conductance auxin transport route down stems dominated by the auxin export protein PIN-FORMED1 (PIN1), has been the focus for understanding long range auxin transport in the shoot. However, recently additional auxin exporters with important roles in the shoot have been identified, including PIN3, PIN4 and PIN7. These proteins contribute to a wider less polar stem auxin transport regime, which we have termed connective auxin transport (CAT), because of its role in communication across the shoot system. Here we present a genetic analysis of the role of CAT in shoot branching. We demonstrate that in Arabidopsis, CAT plays an important role in strigolactone-mediated shoot branching control, with the triple pin3pin4pin7 mutant able to suppress partially the highly branched phenotype of strigolactone deficient mutants. In contrast, the branchy phenotype of mutants lacking the axillary meristem-expressed transcription factor, BRANCHED1 (BRC1) is unaffected by pin3pin4pin7. We further demonstrate that mutation in the ABCB19 auxin export protein, which like PIN3 PIN4 and PIN7 is widely expressed in stems, has very different effects, implicating ABCB19 in auxin loading at axillary bud apices.

OsPIN9, an auxin efflux carrier, is required for the regulation of rice tiller bud outgrowth by ammonium

“…Of the eight PIN members (AtPIN1‐8) identified in the Arabidopsis genome (Gälweiler et al ., 1998; Müller et al ., 1998; Friml et al ., 2002a,b; Mravec et al ., 2009; Ding et al ., 2012; Simon et al ., 2016), five genes ( AtPIN1–4 and AtPIN7 ) are localised in the plasma membrane and strongly support PAT. Until recently, it had been proposed that the PAT stream dominated by AtPIN1 provided a high conductance auxin transport route down stems; AtPIN3 , AtPIN4 and AtPIN7 are likely to be important for communication between the axillary meristems and the main stem PIN1‐dominated PAT stream (Bennett et al ., 2016; van Rongen et al ., 2019). By contrast, for the 12 putative OsPINs in the rice genome, seven PIN genes have already been characterised in rice, in which OsPIN1a–d , OsPIN2 and OsPIN5b are involved in rice tiller growth.…”

“…One proposed mechanism by which auxin in PAT could inhibit buds indirectly is by regulating the synthesis of second messengers, such as strigolactones, which can move into buds to modulate their activity (Brewer et al ., 2009). Another explanation is that cellular PIN differentiation in the stem of the axillary shoot establishes auxin canalisation, leading to sustained outgrowth of the axillary shoot (Ongaro & Leyser, 2008; Prusinkiewicz et al ., 2009; Bennett et al ., 2016; van Rongen et al ., 2019).…”

CsBRC1 inhibits axillary bud outgrowth by directly repressing the auxin efflux carrier CsPIN3 in cucumber

“…4), while PIN3 does not contain BRC1 binding elements in Arabidopsis. Second, CsPIN3 transcripts were enriched in lateral buds of cucumber ( respectively, in regulating rosette branching (18,40,47). In cucumber, however, the shoot apical meristem produces leaves with elongated internodes throughout the life cycle, and only 1 type of shoot branches (similar to cauline branches in Arabidopsis) emerges from the leaf axil of each node.…”

Overcoming Physiological Bottlenecks of Leaf Vitality and Root Development in Cuttings: A Systemic Perspective

“…In intact plants, IAA is synthesized in young expanding leaves and is in the stem either transported root-ward by polar auxin transport (PAT) in xylem parenchyma and cambium cells or co-transported in the phloem associated with assimilate transport (AT) ( Kramer and Bennett, 2006 ; Petrasek and Friml, 2009 ; Leyser, 2011 ; van Rongen et al, 2019 ), while in leaves both pathways can be interconnected ( Cambridge and Morris, 1996 ; Figure 1 ). These auxin routes are supplemented with a low conductance and less polar “connective auxin transport,” linking the PAT route to the surrounding tissues ( Bennett et al, 2016 ; van Rongen et al, 2019 ).…”

“…In intact plants, IAA is synthesized in young expanding leaves and is in the stem either transported root-ward by polar auxin transport (PAT) in xylem parenchyma and cambium cells or co-transported in the phloem associated with assimilate transport (AT) ( Kramer and Bennett, 2006 ; Petrasek and Friml, 2009 ; Leyser, 2011 ; van Rongen et al, 2019 ), while in leaves both pathways can be interconnected ( Cambridge and Morris, 1996 ; Figure 1 ). These auxin routes are supplemented with a low conductance and less polar “connective auxin transport,” linking the PAT route to the surrounding tissues ( Bennett et al, 2016 ; van Rongen et al, 2019 ). In shoot tip cuttings, PAT has important functions in auxin translocation toward the SB and, depending on the plant genotype and environmental condition, cutting leaves of different age may constitute important auxin sources ( Guerrero et al, 1999 ; Garrido et al, 2002 ; Ahkami et al, 2013 ; Yang et al, 2019 ; Figure 1 ).…”